Gas exchanges and photochemical efficiency of West Indian cherry cultivated with saline water and potassium fertilization/Trocas gasosas e eficiencia fotoquimica da aceroleira cultivada com aguas salinas e adubacao potassica.
West Indian cherry (Malpighia emarginata D.C.) is a fruit crop that has stood out as an excellent natural source of vitamin C, besides anthocyanins and carotenoids, compounds with beneficial effects on human health due to their recognized antioxidant action (Maciel et al., 2010). According to Freitas et al. (2006), Brazil is the largest producer, consumer and exporter of this fruit in the world, and its Northeast region stands out as the region were West Indian cherry is best adapted to, due to the conditions of soil and climate.
In the Northeast region, West Indian cherry production reaches 22,964 tons in an area of 7,237 ha, which represents about 70% of the Brazilian production (Caetano, 2010). Thus, the cultivation of West Indian cherry becomes highly promising in the Northeast region, having good prospects for the fruit grower market. Despite the good adaptability of West Indian cherry, the Brazilian semi-arid region poses risks to its cultivation, due to the scarcity of water resources, where the available sources of water for irrigation commonly have high concentrations of salts, especially sodium (Jiang et al., 2012; Souza et al., 2017).
The excess of salts in the soil causes reduction in the osmotic potential, resulting in water deficit in the crops. This deficit causes stomatal closure, limiting C[O.sub.2] assimilation and transpiration in plants, and consequently reduces their photosynthetic rate (Silva et al., 2010). In addition, plants subjected to saline stress undergo changes in the functional state of the thylakoid membranes of chloroplasts, which cause alterations in the characteristics of the fluorescence signals (Chaum & Kirmanee, 2011; Silva et al., 2011a; Freire et al., 2014), thus diminishing growth and yield (Sousa et al., 2012).
As a consequence, in an attempt to mitigate the deleterious effects caused on crops by the excess salts present in irrigation water and/or soil, some management practices have been developed. These practices include fertilization based on the use of fertilizers which favor the acquisition of nutrients by plants under saline conditions (Silva et al., 2011b). Works conducted by Gurgel et al. (2005, 2010) concluded that potassium (K) fertilization led to a decrease in the deleterious effects of irrigation with high-salinity water on the melon crop.
The beneficial effect of potassium is due to the fact that it is vital for photosynthesis, so that situations of deficiency cause reduction in the photosynthetic rate and increase in respiration. In addition, this nutrient favors the formation and translocation of carbohydrates, improving fruit quality (Araujo et al., 2012). Although the benefits of K fertilization are known, studies providing evidence of its mitigating action under conditions of saline stress on plants, mainly in West Indian cherry, are still scarce in the literature. Therefore, this study aimed to evaluate the influence of K fertilization as a mitigating factor of saline stress on gas exchanges and photochemical efficiency of West Indian cherry.
Material and Methods
The experiment was carried out under greenhouse conditions from July 2016 to July 2017, in recipients adapted as drainage lysimeters, at the Center of Technology and Natural Resources of the Federal University of Campina Grande (CTRN/UFCG), located in the municipality of Campina Grande--PB, Brazil (7[degrees] 15' 18" S; 35[degrees] 52' 28" W; ~550 m).
The experimental design was in randomized blocks, with three replicates, using a 2 x 4 factorial scheme, and treatments consisted of two levels of irrigation water electrical conductivity -ECw (0.8 and 3.8 dS [m.sup.-1]) and four K doses (50, 75, 100 and 125% of recommendation). The 100% dose corresponded to 19.8 g of [K.sub.O] [plant.sup.-1] [year.sup.-1] (Musser, 1995).
The lysimeters were filled using a 1-kg layer of crushed stone no. 0, followed by 250 kg of a sandy loam eutrophic Regolithic Neosol, properly pounded to break up clods, from the rural area of the municipality of Esperanza, PB, whose chemical and physical characteristics were obtained according to the methodologies proposed by Claessen (1997): [Ca.sup.2+] = 9.07 [cmol.sub.c] [kg.sup.-1]; [Mg.sup.2+] = 2.78 [cmol.sub.c] [kg.sup.-1]; [Na.sup.+] = 1.64 [cmol.sub.c] [kg.sup.-1]; K+ = 0.23 [cmol.sub.c] [kg.sup.-1]; [H.sup.+] + [Al.sup.3+] = 8.61 [cmol.sub.c] [kg.sup.-1]; [Al.sup.3+] = 0 [cmol.sub.c] [kg.sup.-1]; CEC = 22.33 [cmol.sub.c] [kg.sup.-1]; organic matter = 2.93 dag [kg.sup.-1]; P = 39.8 mg [kg.sup.-1]; pH in water (1:2.5) = 5.58; electrical conductivity of the saturation extract = 2.15 dS [m.sup.-1]; SAR = 0.67 [(mmol [L.sup.-1]).sup.05]; exchangeable sodium percentage = 7.34%; sand = 659.9 g [kg.sup.-1]; silt =161.2 g [kg.sup.-1]; clay = 178.9g [kg.sup.-1]; water content at 33.42 and 1519.5 kPa = 25.91 and 12.96 dag [kg.sup.-1], respectively.
The bottom of each lysimeter was connected to a 4-mm diameter hose to drain the leachate into a container, in order to evaluate the drained water and determine water consumption by plants. The tip of the drain inside the pot was involved with a nonwoven geotextile (Bidim OP 30) to avoid clogging by soil particles.
The experiment used West Indian cherry seedlings, cultivar BRS 366-Jaburu, grafted onto locally developed rootstocks from the Embrapa Tropical Agroindustry, Pacajus, CE. At transplantation, seedlings were 240 days old. During the acclimation period in the greenhouse, plants were irrigated with low-salinity water (0.8 dS [m.sup.-1]). The cultivar BRS 366-Jaburu stands out for its high yield (57 t [ha.sup.-1]) and production of ascorbic acid (2,648 mg 100[g.sup.-1]). These plants are about 1.87 m tall with crown diameter of 2.18 m. Fruits are shiny when ripe, weighing on average 4 to 5 g when unripe, adequate stage to obtain vitamin C, and 6 to 7 g after ripening (EMBRAPA, 2012).
Prior to seedling transplantation, the soil was brought to field capacity using the respective water of each treatment. After transplantation, irrigation was carried out every day by applying in each lysimeter a water volume to maintain the soil near field capacity, and the applied volume was determined according to the water requirement of the plants, estimated by the water balance: volume applied minus the volume drained in the previous irrigation, plus a leaching fraction of 0.10, applied at intervals of 30 days.
Water with electrical conductivity of 3.8 dS [m.sup.-1] was prepared by dissolving the salts NaCl, Ca[Cl.sub.2].2[H.sub.2]O and Mg[Cl.sub.2].6[H.sub.2]O, at equivalent proportion of 7:2:1, respectively, in public-supply water (ECw = 1.40 dS [m.sup.-1]) in the municipality of Campina Grande, PB, based on the relationship between ECw and concentration of salts (10 * [mmol.sub.c] [L.sup.-1] = ECw dS [m.sup.-1]), according to Richards (1954). On the other hand, the ECw level of 0.8 dS [m.sup.-1] was prepared by mixing rainwater (ECw = 0.02 dS [m.sup.-1]) in the municipal-supply water (ECw = 1.40 dS [m.sup.-1]).
Fertilization with phosphorus, potassium and nitrogen was carried out as recommended by Musser (1995), applying the equivalent to 250, 33 and 53 g plant-1 year-1, respectively, of single superphosphate, potassium chloride and urea. Phosphorus was applied all at planting. Nitrogen and potassium were split into 12 portions, applied monthly. In order to prevent probable deficiencies in micronutrients, West Indian cherry plants received every week 5 L of solution containing 1.5 g [L.sup.-1] of Ubyfol [N (15%); [P.sub.2][O.sub.5] (15%); [K.sub.O] (15%); Ca (1%); Mg (1.4%); S (2.7%); Zn (0.5%); B (0.05%); Fe (0.5%); Mn (0.05%); Cu (0.5%); Mo (0.02%)].
Gas exchanges were evaluated in the middle third of the crown of West Indian cherry plants during the transition from flowering to fruiting (at 180 days after transplanting), based on the following parameters: stomatal conductance (gs--mol [H.sub.2]O [m.sup.-2] [s.sup.-1]), C[O.sub.2] assimilation rate (A) ([micro]mol [m.sup.-2] [s.sup.-1]), transpiration (E) (mmol [H.sub.2]O [m.sup.-2] [s.sup.-1]) and internal C[O.sub.2] concentration (Ci) ([micro]mol [mol.sup.-1]) using a portable infrared gas analyzer (IRGA), model LCPro+ Portable Photosynthesis System*. After collection, these data were used to quantify instantaneous water use efficiency (WUEi) (A/E) [(gmol [m.sup.-2] [s.sup.-1]) [(mmol [H.sub.2]O [m.sup.-2] [s.sup.-1]).sup.-1]] and intrinsic carboxylation efficiency (EiCi) (A/Ci) [(gmol [m.sup.-2] [s.sup.-1]) [([micro]mol [mol.sup.-1]).sup.-1]]. Initial fluorescence (Fo), maximum fluorescence (Fm), variable fluorescence (Fv) and potential quantum efficiency (Fv/Fm) were also measured in leaves pre-adapted to dark using leaf clips for 30 min, between 7 and 8 a.m., using a modulated fluorometer Plant Efficiency Analyser--PEA II*.
The data were subjected to analysis of variance by F test and, when significant, means were compared by Tukey test at 0.05 probability level for water salinity levels and regression analysis was conducted for K doses, using the statistical program SISVAR-ESAL (Ferreira, 2011).
Results and Discussion
There was significant influence (p < 0.05) of the interaction between levels of irrigation water salinity and K fertilization on variable fluorescence (Fv). The other parameters of gas exchanges and chlorophyll a fluorescence were only significantly influenced (p < 0.05) by the irrigation water salinity, except the instantaneous water use efficiency (WUEi), which was not significantly affected by any of the factors studied. Potassium doses significantly influenced (p < 0.05) only the variable fluorescence (Table 1).
Irrigation water salinity of 3.8 dS [m.sup.-1] negatively affected gas exchanges in West Indian cherry, leading to accentuated reductions of the order of 47.58, 33.14, 41.03 and 56.75% in stomatal conductance, transpiration, C[O.sub.2] assimilation rate and instantaneous carboxylation efficiency, respectively, in comparison to the ECw level of 0.8 dS [m.sup.-1] (Figures 1A, B, C and E). However, internal C[O.sub.2] concentration increased by 38.03% as a function of the increment in ECw levels from 0.8 to 3.8 dS [m.sup.-1] (Figure 1D). According to Freire et al. (2014), such increment in Ci inside the leaves indicates that C[O.sub.2] is not being used for the synthesis of sugars in the photosynthetic process, suggesting that probably a non-stomatal factor was interfering with this process, which can be confirmed by the reduction in the photosynthetic rate of plants irrigated with 3.8 dS [m.sup.-1] water (Figure 2A). Despite the drastic reduction in stomatal conductance, and consequently in transpiration, it did not influence the instantaneous water use efficiency or internal C[O.sub.2] concentration, since there was no reduction in C[O.sub.2] influx in plants irrigated with high-salinity water.
Thus, the reduction in stomatal conductance can be related to the tolerance mechanism of the species, aiming to reduce water loss and consequently the absorption of water and salts from the soil solution, without compromising photosynthetic activity. According to Taiz & Zeiger (2013), plants under salt stress have as the first response to salinity the reduction in stomatal opening, to reduce water loss through the leaves, which is induced by the reduction in the osmotic potential of the soil solution, resulting in higher resistance to water absorption by the roots. Accumulation of salts in the leaves also affects, significantly, essential physiological processes, including gs (Hussain et al., 2012).
The reductions observed in C[O.sub.2] assimilation rate and intrinsic carboxylation efficiency coincided with the increase in internal C[O.sub.2] concentration of plants cultivated under high salinity (Figures 1C, D and E). Reductions in intrinsic carboxylation efficiency are related to metabolic restrictions in the Calvin cycle, where the received carbon is not being fixed in the carboxylation stage in mesophyll cells (Larcher, 2006; Sousa et al., 2016). According to Taiz & Zeiger (2013), as the stress becomes severe there is a dehydration in mesophyll cells, the mesophyll metabolism is damaged and, consequently, carboxylation efficiency is compromised. This result is an indication that non-stomatal factors act on the photosynthetic activity of West Indian cherry, such as low activity of the enzyme Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), probably due to the low availability of substrate (ATP and NADPH) for activation and regeneration of the enzyme, which come from the photochemical phase of photosynthesis, leading to reduction in C[O.sub.2] carboxylation and increase in its internal concentration (Hussain et al., 2012; Silva et al., 2015; Sa et al., 2017).
Initial fluorescence (Fo) and maximum fluorescence (Fm) of West Indian cherry were reduced by 21.49 and 15.48% as water salinity increased from 0.8 to 3.8 dS [m.sup.-1] respectively (Figures 2A and B). Initial fluorescence is characterized as the minimum fluorescence emitted when all reaction centers, dark adapted, are open (Gorbe & Calatayud, 2012). Maximum fluorescence is an indicator that represents the maximum intensity of the fluorescence emitted, when almost all quinone is reduced and the reaction centers reach their maximum capacity of photochemical reactions (Suassuna et al., 2010; Silva et al., 2015). The reduction in initial and maximum fluorescence indicates reduction in the photochemical capacity of West Indian cherry under saline stress conditions, which combined with the low C[O.sub.2] carboxylation efficiency confirms that the low photosynthetic yield of this crop under high salinity results from the damages caused by the excess of salts to the chlorophyll a, reducing its activity and thus the synthesis of ATP and NADPH.
Variable fluorescence in West Indian cherry plants irrigated with low-salinity water (0.8 dS [m.sup.-1]) decreased linearly as K doses increased, with a reduction of 22.78% in the Fv in plants fertilized with 125% of the K recommendation in comparison to those subjected to 50%, which represents a reduction of 162.50 electrons [quantum.sup.-1] (Figure 3A). In plants irrigated with high-salinity water (EC = 3.8 dS [m.sup.-1]) there was a quadratic behavior for variable fluorescence (Figure 3A), and highest Fv was obtained when plants were fertilized with K dose of 87% (501.93 electrons [quantum.sup.-1]). From this dose on, the increment in K fertilization led to reduction in this variable and corresponded to 362.145 electrons [quantum.sup.-1] at the highest K dose, which represents a decrease of 139.79 electrons [quantum.sup.-1]. Such initial increase in Fv due to the increment in K dose is related to the greater competition of this cation with other ions, such as Na ions, thus reducing the deleterious effects of saline stress on chlorophyll a activity. However, as the dose increased, K may have intensified even more the salt stress.
As previously observed for Fo and Fm (Figures 2A and B), the potential quantum efficiency of photosystem II (Figure 3B) also decreased with the increase in salinity, and irrigation with high-salinity water (3.8 dS [m.sup.-1]) caused reduction in the Fv/Fm ratio from 0.75, in plants irrigated with 0.8 dS [m.sup.-1], to 0.63 electrons [quantum.sup.-1]. The Fv/Fm ratio reflects the efficiency relative to the absorption of light energy by the antenna complex of the PSII and to its conversion into chemical energy, being considered as a sensitive indicator of photosynthetic performance of the plant, as well as an indicator of disturbances in the photosynthetic system caused by stresses and its reduction consists in the limitation of photochemical activity (Lucena et al., 2012). Fv/Fm values between 0.75 and 0.85 electrons [quantum.sup.-1] suggest that the photosynthetic apparatus is intact, as opposed to values lower than 0.75 electrons [quantum.sup.-1] (Reis & Campostrini, 2011; Silva et al., 2015). Therefore, it can be inferred that the photosynthetic apparatus of West Indian cherry plants irrigated with 3.8 dS [m.sup.-1] water (Figure 3B) is compromised by salt stress, since these plants had Fv/Fm values of 0.63 electrons [quantum.sup.-1].
1. Irrigation using water with electrical conductivity of 3.8 dS [m.sup.-1] compromises gas exchanges and photochemical efficiency of West Indian cherry plants.
2. Potassium fertilization was not efficient at reducing the stress caused by the studied level of water salinity.
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Adaan S. Dias (1), Geovani S. de Lima (2), Francisco V. da S. Sa (3), Hans R. Gheyi (4), Lauriane A. dos A. Soares (2) & Pedro D. Fernandes (1)
(1) Universidade Federal de Campina Grande/Centro de Tecnologia e Recursos Naturais/Programa de Pos-Graduacao em Engenharia Agricola. Campina Grande, PB. E-mail: firstname.lastname@example.org--ORCID: 0000-0002-2247-1511; email@example.com--ORCID: 0000- 0001-5070-1030
(2) Universidade Federal de Campina Grande/Centro de Ciencias e Tecnologia Agroalimentar/Programa de Pos-Graduacao em Horticultura Tropical. Pombal, PB. E-mail: firstname.lastname@example.org--ORCID: 0000-0001-9960-1858 (Corresponding author); email@example.com--ORCID: 0000-0002-7689-9628
(3) Universidade Federal Rural do Semi-Arido/Centro de Ciencias Agrarias/Programa de Pos-Graduacao em Manejo de Solo e Agua. Mossoro, RN. E-mail: firstname.lastname@example.org--ORCID: 0000-0001-6585-8161
(4) Universidade Federal do Reconcavo da Bahia/Nucleo de Engenharia de Agua e Solo. Cruz das Almas, BA. E-mail: email@example.com--ORCID: 0000 0002-1066-0315
Ref. 185978-Received 30 Sept, 2017 * Accepted 22 Mar, 2018 * Published 25 Jul, 2018
Table 1. Summary of the F test for stomatal conductance (gs), transpiration (E), C[O.sub.2] assimilation rate (A), internal C[O.sub.2] concentration (Ci), intrinsic carboxylation efficiency (EiCi), instantaneous water use efficiency (WUEi), initial fluorescence (Fo), maximum fluorescence (Fm), variable fluorescence (Fv) and potential quantum efficiency (Fv/Fm) of West Indian cherry plants irrigated with saline water and fertilized with potassium doses at 180 days after transplanting Source of variation F test gs E A Ci EiCi Saline levels (SL) ** ** ** ** ** Doses of K (DK) ns ns ns ns ns Linear Regression -- -- -- -- -- Quadratic Regression -- -- -- -- -- Interaction SL*DK ns ns ns ns ns Blocks ns ns ns ns ns CV (%) 21.91 25.16 22.51 25.15 10.00 Source of variation F test WUEi Fo Fm Fv Fv/Fm Saline levels (SL) ns ** ** ** ** Doses of K (DK) ns ns ns * ns Linear Regression -- -- -- * -- Quadratic Regression -- -- -- * Interaction SL*DK ns ns ns * ns Blocks ns ns ns ns ns CV (%) 36.33 14.76 7.33 11.64 3.86 ns, **, * Respectively not significant, significant at p < 0.01 and p < 0.05 Figure 1. Stomatal conductance--gs (A), transpiration--E (B), C[O.sub.2] assimilation rate--A (C), internal C[O.sub.2] concentration--Ci (D) and intrinsic carboxylation efficiency--CEi (E) of West Indian plants irrigated with saline water at 180 days after transplanting Water salinity (dS [m.sup.-1] gs(mol [H.sub.2]O [m.sup.-2][s.sup.-1]) A. 0.8 0.124 a 3.8 0.065 b E(mmol [H.sub.2] [Om.sup.-2][S.sup.-1]) B. 0.8 0.243 a 3.8 0.831 b A([mu]mol) [m.sup.-2][s.sup.-1] 0.8 7.369 a 3.8 4.345 b Ci([mu]mol) [mol.sup.-1]) D. 0.8 201.83 a 3.8 278.58 b EiCi[([mu]mol] [mol.sup.-1]).sup.-1] E. 0.8 0.037 a 3.8 0.016 b Note: Table made from bar graph. Figure 2. Initial fluorescence--Fo (A) and maximum fluorescence--Fm (B) of West Indian cherry plants irrigated with saline water at 180 days after transplanting Water salinity (dS [m.sup.-1] Fo(electrons [quantum.sup.-1]) A. 0.8 252.41 a 3.8 198.16 b F(mmol (electrons [quantum.sup.-1]) B. 0.8 715.91 a 3.8 605.08 b Note: Table made from bar graph. Figure 3. Variable fluorescence--Fv (A) as a function of the interaction between irrigation water salinity and potassium doses, and potential quantum efficiency of photosystem II--Fv/Fm (B) of West Indian cherry plants irrigated with saline water at 180 days after transplanting Water salinity (dS [m.sup.-1] Fv/Fm (electrons [quantinum.sup.-1]) B. 0.8 0.748 a 3.8 0.630 b Note: Table made from bar graph.